Versions
of this paper orignally appeared in the New Science Magazine, Whales
and Ethics (1992) 11 Essays on Whales and Man, (1994)

Brains, Behaviour and
Intelligence in Cetaceans
(Whales, Dolphins and Porpoises)

- Margaret Klinowska
-
Research Group in Mammalian Ecology and Reproduction,
Physiological Laboratory, Cambridge University

Introduction
It is widely believed that cetaceans (the whales, dolphins and porpoises) are
highly "intelligent". Probably the major historical basis for this
dogma is the size and complex surface appearance of cetacean brains (Figure
1 ). The idea that brain size and surface characteristics are related to "intelligence"
was widespread among neuroanatomists around the turn of the century, but received
a severe blow when it was found that the brains of several distinguished people
(who had bequeathed their bodies to science) showed no outstanding characteristics
whatever and were, in fact, disappointingly ordinary (Kuhlenbeck,1978). This
was just as well, as elements of such work were being badly misused to justify
repressive racist, anti- feminist and colonial attitudes. The subject remained
generally out of fashion until John Lilly, a medical doctor by training, became
impressed by the absolute size of cetacean brains. His famous book "Mind
in the Waters" (Lilly,1967) appears to have led to much of the modern interest
in this topic.We all know in a general way what we mean by "intelligence"
but unfortunately, it is so difficult to define strictly that, even when it
comes to devising comparative tests for humans, all kinds of problems arise.
The problems in defining "intelligence" in such a way that valid comparisons
can be made across a wide of range of species have yet to be overcome, although
this has not deterred a great deal of research into the subject.

Brain Quantity
If "intelligence" was simply determined by absolute brain size, there
would be no difficulty in deciding which species was top (Table 1 ).

But as the species with the biggest brains also tend to be the ones with the
biggest bodies, it might be that large animals just need larger brains to control
and maintain their larger bodies. Even when we talk of "intelligence"
in a general way, we mean something more than the sum of body control systems.
A simple way to make allowance for different body weights is to express brain
weight as a percentage of body weight (Table 2).

In this list humans
are seen to have a great advantage over the others, and we also have a very
different view of the large whales. Of course, these are only very limited lists
to illustrate this type of approach to the problem.

Researchers have
made far more extensive and sophisticated attempts to investigate comparative
intelligence in this way. There is, however, a basic problem in compiling lists
of this type, and that is deciding which weights to take as typical of a species.
For example, normal humans can have brains weighing anything between 900 and
2,000 grams. The weight of an individual brain will also vary depending on whether
it is fresh or preserved, and on exactly which parts are included. Body weight
varies greatly between individuals, and i n some whale species the weight of
individual animals can vary by about 40% over a year because of their seasonal
feeding habits. The brain weight to body weight relation- ship varies with age
young mammals have proportionally smaller bodies and larger heads, and brain
size decreases significantly in old age. There can be marked sex differences
in body size, for example adult female baleen whales in many species are much
larger than males, while in sperm whales it is the adult males which are much
larger than the females. Normal variations in brain and body size have only
been well studied in a, few species, and usually a researcher seeking to compile
extensive brain and body weight lists has no choice but to take whatever specimens
are available, regardless of whether the material is really representative of
the species as a whole.

Some of the most
extensive modern comparative studies have been made by Jerison (e.g.1978), who
has developed an index, the encephalization quotient (EQ), to express the brain
weight/body weight relationship. His studies do show some cetaceans (e.g. toothed
whales like the killer whale and sperm whale) with an EQ similar to humans.
However, other studies conclude that relative brain size is not necessarily
related to "intelligence". Pilleri, Gihr and Kraus (1985) made an
exhaustive study of rodent brain size in relation to behaviour and concluded
that "intelligence", whether human or animal, is not a unified brain
function, but one which is too complex to be characterised with a single numerical
index. They found that cerebral quotients (various ways of expressing relative
brain and body size) are generally inconclusive as criteria for mammalian "intelligence".

Macphail (1982),
in an extensive review of brain and behaviour in vertebrates, also found that
brain size and characteristics were unsatisfactory indicators of "intelligence",
because there are too many anomalies. A particular example is the spiny anteater
(an egg laying mammal, related to the duck-billed platypus), with a neocortex
(the so-cal led 'modern' part of the brain, which is greatly developed i n primates
and humans) relatively much larger than that of a human. Despite this endowment,
nobody has so far put forward any claims for superior "intelligence"
in spiny anteaters.

Another problem
with the search for a comparative measure of "intelligence" through
brain quantity is addressed in the volume edited by Hahn, Jensen and Dudek (1979).
Although a number of the papers deal with laboratory species selected and bred
for increased brain size, there is extraordinary difficuIty in demonstrating
any improvement in performance on a variety of tests either within or between
species.

The degree of convolution
or folding of the cortical brain surface has often in the past been taken as
an absolute indicator of "intelligence". However, more recent work
regards this as simply a mechanical reflection of an increase in neocortical
volume. Jerison (1979), for example, regards degree of convolution and absolute
brain size as equivalent measures, speculating that the extra volume is required
to accommodate increasingly complex connections between the brain cells. Ridgway
(1986) presents evidence from a variety of sources to show that bottlenose dolphins
have a much higher index of folding than humans. However, as Ridgway (1986)
also explains, the neocortex of the cetacean brain is relatively thin - about
half that of humans - giving a total average dolphin neocortical volume about
80% of that of humans. Also, as explained in more detail below, cetacean neocortical
structure is generally very much simpler than that of land mammals, and does
not therefore conform to the assumptions that more convoluted neocortices are
necessarily more voluminous or more complex. This is not the only anomaly, for
example compare the convoluted appearances of the horse and chimpanzee brains.

Brain Quality
Another school of thought (e.g. Holloway,1979), finds the consideration of brain
and body sizes alone insufficient, indeed "trivial", and emphasises
the importance of the evolutionary changes in brain organisation. Holloway (1979)
goes on to demonstrate that brain weight is a poor predictor of the internal
structural complexity which he believes to be the most important factor in the
evolution of "intelligence".

Studies of the
internal structure of carefully preserved dolphin brains using a variety of
techniques (e.g. Kesarev, Malofeyeva and Trykova, 1977; Morgane, Jacobs and
Galaburda, 1986; Garey and Revishchin, 1990; Glazer, Morgane and Leranth, 1990)
show that these animals have not developed the latest stage of brain evolution,
characteristic of land mammals. It is thought that this line of evolution began
about 50 million years ago in land mammals, whereas the cetacean ancestors returned
to the water some 70 million years ago, well before this stage was reached.
Although the cetacean brain has not followed the course of evolution of the
land mammals, it does retain all the conservative characteristics seen in primitive
land forms, such as hedgehogs and bats. The dolphin brain shows none of the
anatomical structural heterogeneity characteristic of more evolved brains such
as those of primates, but the regions of the neocortex can be differentiated
by electrophysiological methods, and are arranged in very much the same order
as in the hypothetical ancestor of mammals (Supin, Mukhametov, Ladygina, Popov,
Mass and Poliakova, 1978).

The neocortex is
the part of the brain which most clearly differentiates mammals from non-mammals,
and there is a wide belief that the growth of the neocortex is responsible for
the evolution of "intelligence". The anatomical characteristics of
mammalian neocortex are that it has six layers and that different functional
areas (e.g. that dealing with vision) have somewhat different organisation of
these layers. The anatomical studies cited above demonstrate that cetaceans
only have five layers in the neocortex (layer IV is missing) and that there
is no anatomically different organisation of these Iayers according to function.
In some views (e.g. Kesarev et al.,1977) this means that cetaceans have no true
neocortex, or only a preneocortex. If a neocortex is really essential for the
development of "intelligence", cetaceans are clearly disqualified.
However, Macphail (1982) comprehensively demolishes the idea of a special role
for the neocortex in "intelligence".

Behaviour
Yet another school of thought believes that the significance of the relative
size or structural complexity of brains needs to be validated by behavioural
data before any assumptions can be made about their role in the development
of "intelligence". While a variety of laboratory tasks have been used,
that of learning set formation (the inter-problem improvement in performance
seen in subjects given a series of discriminations involving different pairs
of stimuli) has been widely explored since Harlow (1949) concluded that the
results reflected evolutionary relationships.

Unfortunately,
subsequent work showed that closely related species may have widely divergent
performances, and that some "lower" species may equal or excel "higher"
species. Further , the ordering of species does not agree with that predicted
from relative brain size (EQ) (Table 3).

Macphail (1982)
remarks that it is not clear that any of the differences in performance in learning
set formation (or any of the other types of behavioural studies considered)
observed are due to differences in intellectual capacity, and he cites a number
of studies which demonstrate, as might be expected, that relative species performance
is very dependent on detaiIs of experimental technique.

While all non-human
animals have ways of communicating with each other, for example by body language,
sounds, touch or chemicals, they have not developed anything of comparable versatility
to human language. Although many attempts have been made, no non-human has yet
been taught more than the rudiments of human-type language. Macphail (1982)
describes the experiments and species (chimpanzee, gorilla, bottlenose dolphin,
California sea lion, pigeon) concerned, and argues that such performances to
date are better described as ordering responses sequentially for reward, rather
than as real steps on the road to language. He also puts forward an interesting
interpretation of the human capacity for problem solving, which is quite beyond
the capacity of any non-human. If humans solve problems, directly or indirectly,
with the aid of language, the superiority of humans in problem solving might
simply reflect the possession of language, and the capacity for language, in
turn might be a species-specific specialisation, independent of general "intelligence".

Discussion
Clearly, the cetacean type of mammalian brain is sufficient for the purpose,
but it is anatomically simple and lacks the new structures which are conventionally
associated with the development of "intelligence" among land mammals.
However, as we have seen, there are good reasons for questioning these conventions.

Dolphin brains
are relatively large, but again there are reasons for questioning the assumption
that brain size is related to "intelligence". Crick and Mitchison's
(1983) theory of the function of dream sleep may provide an alternative explanation
for such anomalously large brains. They propose that rapid-eye-movement sleep
(REM or dream or paradoxical sleep) acts to remove undesirable interactions
in networks of cells in the cerebral cortex. They call this process, which is
the opposite of learning, but different from forgetting, "reverse learning".
Animals which cannot use this system need another way to avoid overloading the
neural network, for example by having bigger brains. The spiny anteater and
dolphins are the only mammals so far tested which do not have REM sleep (Allison,
Van Twyner and Goff, 1972; Mukhametov, 1984) - and they also have disproportionally
large brains. So, following this line of reasoning, dolphins and spiny anteaters
would have to have big brains because they cannot dream.

The behaviour of
dolphins is frequently cited as evidence for high "intelligence".
The capacity of some smaller cetacean species (not all see Defran and Pryor,
1980) to learn performance tricks in captivity is often taken as "proof"
of cetacean intelligence, but many other animals from elephants to fleas can
achieve such feats, without this being taken as evidence for a special order
of "intelligence". People who have been in close contact with dolphins
and whales often speak of a feeling that they are with an "intelligent"
animal , but many dog-owners, for example, have a close rapport with their pets
and also speak of "intelligence" and an ability to "understand
every word I say". The complexity of cetacean societies is another point
frequently cited, but ants and bees, for example, have indisputably complex
societies and we do not usually acknowledge these creatures as highly "intelligent".
What about the cetacean's "sophisticated communication abilities"?
We still know very little about the social significance of many of their sounds
(excluding echo-location, which is only an aid for hunting and exploring the
environment), body language and other communication systems, but in general
the repertoire is far too limited to provide anything like our kind of "language".
Experiments have shown that some dolphins may have the rudimentary skills necessary
for understanding and use of language, but these skills seem fairly common,
and have so far been found in a range of species including pigeons, pinnipeds
and apes. Again, what could be more "sophisticated" than the multiple
communication systems of bees? And how do we usually regard bees?

Friendliness and
helpfulness towards people are often discussed, but are we flattering ourselves
in believing that the animals really "intended" to help? For perhaps
obvious reasons we hear less of unhelpful behaviour, but there are well- documented
cases. Many species of wild animals have been tamed or habituated to humans.
Sometimes such animals become a danger to themselves or to people. Even tamed
wild dolphins can become a considerable nuisance (for example setting boats
adrift by pulIing up anchors) and sometimes dangerous. Instancesof "friendly"
dolphins attacking swimmers (apparently unprovoked) are well documented, as
are instances of swimmers being pushed out to sea, "abducted" or prevented
from re-entering boats and other craft (e.g. Lockyer,1990).

Gaskin (1982) has
concluded that there is abundant evidence that cetaceans communicate information
about "what", "where" and "who". There is no substantive
evidence that they transmit information about "when", "how"
or "why". So with respect to Kipling's (1902) "six honest serving
men" of learning and intellect, cetaceans appear to be three servants short.

Conclusion
There is another less anthropomorphic or "speciesist" way of looking
at the question of general "intelligence". All living species must
be highly "intelligent" in a broad sense in order to survive. From
this point of view, humans are no more and no less than one of the species living
on this planet with particular adaptations (specialised "intelligence")
for their own way of life. This perspective allows us to view the superb professionalism
of all species with equal respect, and not in some artificial ranking order
of higher or lower "intelligence" (with the hidden assumption that
they are more or less worthy of conservation and consideration, and that as
humans are, of course, in the first rank, their wishes have priority).

Dawkins (1980)
recognises that suffering in animals may be difficult to measure and that misinterpretations
of the meaning of animal behaviour can arise from projecting human feelings
on to animals. Being "human-like" or "higher" or "more
intelligent" is considered a poor guide to whether an animal experiences
suffering. Behavioural and physiological evidence are more reliable and, taken
together with information on the treatment of the animals, the situation can
be evaluated. Without this basic preparation, suffering may be seen where there
is none or, worse, may be overlooked because it does not wear a human face.

Thus, while it
is not yet possible to make any final scientific judgements on cetacean "intelligence",
there are sufficient doubts to render the unqual ified perpetuation of the dogma
highly questionable - and possibly even counter- productive in the wider conservation
and animal welfare context.